Halophilic and haloalkaliphilic sulfur-oxidizing bacteria

Abstract

Chemotrophic sulfur-oxidizing bacteria (SOB) represent an important functional group of microorganisms responsible for the dark oxidation of reduced sulfur compounds generated by sulfidogens. Until recently, only a single genus of halophilic SOB (Halothiobacillus) has been described, and nothing was known about the ability of this group to grow at high pH. Investigation of soda lakes, unique extremely alkaline and saline habitats, led to the discovery of a novel ecotype of natronophilic SOB. In contrast to the previously known neutrophilic ecotype, this group cannot grow at neutral pH, but grows optimally in soda brines at pH values around 10. They were the first chemolithoautotrophs among the described alkaliphiles. The group, so far, includes four novel genera within the Gammaproteobacteria. The genera Thioalkalimicrobium and Thioalkalispira represent low salt-tolerant alkaliphiles tolerating up to 1.5 M Na +. The genus Thioalkalibacter is a high salt-tolerant facultative alkaliphile. The genus Thioalkalivibrio is the most diverse and includes aerobic extremely salt-tolerant members and moderately salt-tolerant thiocyanate-utilizing and facultatively anaerobic denitrifying strains. The genome sequence of two Thioalkalivibrio strains revealed the presence of a truncated Sox system lacking the SoxCD component which is typical for gammaproteobacterial SOB. Bioenergetic studies of high salt-tolerant Thioalkalivibrio strains showed an obligate sodium dependence for respiratory activity implying the presence of sodium-dependent elements. Investigation of hypersaline inland chloride-sulfate lakes and hypersaline brines of marine origin with neutral pH revealed an unexpectedly high culturable diversity of halophilic obligately chemolithoautotrophic SOB comprising seven different groups within the Gammaproteobacteria. Two groups of strictly aerobic moderate halophiles were represented by the known genera Halothiobacillus and Thiomicrospira. Under denitrifying conditions and with thiocyanate as e-donor, three novel groups of moderately halophilic SOB were represented by the genera Thiohalomonas, Thiohalophilus, and Thiohalobacter. At 4 M NaCl, two groups of extremely halophilic SOB (a type not known before among the SOB) had been discovered. The obligately aerobic extreme halophiles comprised a novel genus Thiohalospira, and the facultatively anaerobic nitrate-reducing extreme halophiles-A novel deep-lineage genus Thiohalorhabdus. Overall, the investigation of hypersaline and (halo)alkaline habitats uncovered a novel and diverse world of extremophilic SOB with properties previously unknown for chemolithoautotrophic bacteria.